Pregnancy in fish

A pregnant Southern platyfish

Pregnancy has been traditionally defined as the period of time eggs are incubated in the body after the egg-sperm union.[1] Although the term often refers to placental mammals, it has also been used in the titles of many international, peer-reviewed, scientific articles on fish, e.g.[2][3][4][5] Consistent with this definition, there are several modes of reproduction in fish, providing different amounts of parental care. In ovoviviparity, there is internal fertilization and the young are born live but there is no placental connection or significant trophic (feeding) interaction; the mother's body maintains gas exchange but the unborn young are nourished by egg yolk. There are two types of viviparity in fish. In histotrophic viviparity, the zygotes develop in the female's oviducts, but she provides no direct nutrition; the embryos survive by eating her eggs or their unborn siblings. In hemotrophic viviparity, the zygotes are retained within the female and are provided with nutrients by her, often through some form of placenta.

In seahorses and pipefish, it is the male that becomes pregnant.

Types of reproduction and pregnancy

[edit]
Birth of guppy fry

Pregnancy has been traditionally defined as the period during which developing embryos are incubated in the body after egg-sperm union. Despite strong similarities between viviparity in mammals, researchers have historically been reluctant to use the term "pregnancy" for non-mammals because of the highly developed form of viviparity in eutherians. Recent research into physiological, morphological and genetic changes associated with fish reproduction provide evidence that incubation in some species is a highly specialized form of reproduction similar to other forms of viviparity.[1] Although the term "pregnancy" often refers to eutherian animals, it has also been used in the titles of many international, peer-reviewed, scientific articles on fish, e.g.[2][3][4][5]

Five modes of reproduction can be differentiated in fish based on relations between the zygote(s) and parents:[6][7]

  • Ovuliparity: Fertilization of eggs is external; zygotes develop externally.
  • Oviparity: Fertilization of eggs is internal; zygotes develop externally as eggs with large vitellus.
  • Ovoviviparity: Fertilization is internal; zygotes are retained in the female (or male) but without major trophic (feeding) interactions between zygote and parents (there may be minor interactions, such as maintenance of water and oxygen levels). The embryos depend upon their yolk for survival.

There are two types of viviparity among fish.

  • Histotrophic ("tissue eating") viviparity: The zygotes develop in the female's oviducts, but she provides no direct nutrition. The embryos survive by eating her eggs or their unborn siblings.
  • Hemotrophic ("blood eating") viviparity: The zygotes are retained within the female and are provided with nutrients by her, often through some form of placenta.


Diagram

Fish reproduction types

Ovoviviparous fish

[edit]

Examples of ovoviviparous fish are many of the squaliform sharks, which include sand sharks, mackerel sharks, nurse sharks, requiem sharks, dog sharks and hammerheads, among others, and the lobe finned coelacanth. Some species of rockfish (Sebastes) and sculpins (Comephoridae) produce rather weak larvae with no egg membrane and are also, by definition, ovoviviparous.[8][9] Ovoviviparity occurs in most live-bearing bony fishes (Poeciliidae).

Viviparous fish

[edit]

Viviparous fish include the families Goodeidae, Anablepidae, Jenynsiidae, Poeciliidae, Embiotocidae and some sharks (some species of the requiem sharks, Carcharinidae and the hammerheads, Sphyrnidae, among others). The halfbeaks, Hemiramphidae, are found in both marine and freshwaters and those species that are marine produce eggs with extended filaments that attach to floating or stationary debris, while those that are found in freshwater are viviparous with internal fertilization. The Bythitidae are also viviparous although one species, Dinematichthys ilucoeteoides, is reported to be ovoviviparous.[8]

Aquarists commonly refer to ovoviviparous and viviparous fish as "livebearers". Examples include guppies, mollies, moonfish, platys, four-eyed fish and swordtails. All of these varieties exhibit signs of their pregnancy before the live fry are born. As examples, the female swordtail and guppy will both give birth to anywhere from 20 to 100 live young after a gestation period of four to six weeks, and mollies will produce a brood of 20 to 60 live young after a gestation of six to 10 weeks.[10]

Nutrition during pregnancy

[edit]

Other terms relating to pregnancy in fish relate to the differences in the mode and extent of support the female gives the developing offspring.

"Lecithotrophy" (yolk feeding) occurs when the mother provisions the oocyte with all the resources it needs prior to fertilization, so the egg is independent of the mother. Many members of the fish family Poeciliidae are considered to be lecithotrophic, however, research is increasingly showing that others are matrotrophic.[11]

"Aplacental viviparity" occurs when the female retains the embryos during the entire time of development but without any transfer of nutrients to the young. The yolk sac is the only source of nutrients for the developing embryo. There are at least two exceptions to this; some sharks gain nourishment by eating unfertilized eggs produced by the mother (oophagy or egg eating) or by eating their unborn siblings (intra-uterine cannibalism).

"Matrotrophy" (mother feeding) occurs when the embryo exhausts its yolk supply early in gestation and the mother provides additional nutrition.[12] Post-fertilization transfer of nutrients has been reported in several species within the genera Gambusia and Poecilia, specifically, G. affinis, G. clarkhubbsi, G. holbrooki, G. gaigei, G. geiseri, G. nobilis, P. formosa, P. latipinna, and P. mexicana.[11]

Viviparous fish have developed several ways of providing their offspring with nutrition. "Embryotrophic" or "histrotrophic" nutrition occurs by the production of nutritive fluid, uterine milk, by the uterine lining, which is absorbed directly by the developing embryo. "Hemotrophic" nutrition occurs through the passing of nutritive substances between blood vessels of the mother and embryo that are in close proximity, i.e. a placenta-like organ similar to that found in mammals.[8]

Comparison between species

[edit]

There is considerable variation between species in the length of pregnancy. At least one group of fish has been named after its pregnancy characteristics. The surfperch, genus Embiotoca, is a saltwater fish with a gestation period of three to six months.[13] This lengthy period of pregnancy gives the family its scientific name from the Greek "embios" meaning "persistent" and "tokos" meaning "birth".

The table below shows the gestation period and number of young born for some selected fish.[citation needed]

Species Reproduction

method

Gestation period

(Days)

Number of young

(Average)

Atlantic sharpnose shark[14] (Rhizoprionodon terraenovae) Viviparous 300-330 4-6
Barbeled houndshark[15] (Leptocharias smithii) Viviparousa >120 7
Blackspot shark[16] (Carcharhinus sealei) Viviparousb 270 1-2
Blue shark[17] (Prionace glauca) Viviparous 270-366 4-135
Bonnethead shark (Sphyrna tiburo) Viviparousc 4-12[18]
Bull shark[19] (Carcharhinus leucas) Viviparous 366 4-10
Butterfly goodeid[20] (Ameca splendens) Viviparous 55-60 6-30
Caribbean sharpnose shark (Rhizoprionodon porosus) Viviparous 2-6[21]
Daggernose shark[22] (Isogomphodon oxyrhynchus) Viviparous 366 2-8
Lemon shark[23] (Negaprion brevirostris) Viviparous 366 18 (max)
Oceanic whitetip shark[24] (Carcharhinus longimanus) Viviparous 366 1-15
Dwarf seahorse[25] (Hippocampus zosterae) Ovoviviparous 3-55 10
Sandbar shark[26] (Carcharhinus plumbeus) Viviparous 366 8
Spadenose shark[22] (Scoliodon laticaudus) Viviparousd 150-180 6-18
Viviparous eelpout[27] (Zoarces viviparus) Viviparouse 180 30-400
Basking shark[28] (Cetorhinus maximus) Ovoviviparous >366 unknownf
Bat ray[29] (Myliobatis californica) Ovoviviparous 270-366 2-10
Coelacanth (g. Latimeria) Ovoviviparous >366[30]
Blue stingray (Dasyatis chrysonota) Ovoviviparous 270 1-5
Bluespotted stingray[31] (Neotrygon kuhlii) Ovoviviparous 90-150 1-7
Carpet sharks (f. Ginglymostomatidae) Ovoviviparous 180 30-40
Knifetooth sawfish[32] (Anoxypristis cuspidata) Ovoviviparous 150 6-23
Nurse shark (Ginglymostoma cirratum), Ovoviviparous 150 21-29
Sailfin molly (Poecilia latipinna) Ovoviviparous 21-28 10-140
Salmon shark[33] (Lamna ditropis) Ovoviviparous 270 2-6
Sand tiger shark[34] (Carcharias taurus) Ovoviviparous 270-366 2g
School shark[35] (Galeorhinus galeus) Ovoviviparous 366 28-38
Shortfin mako shark[36] (Isurus oxyrinchus) Ovoviviparous 450-540 4-18
Spotted eagle ray[37] (Aetobatus narinari) Ovoviviparous 366 4
Tiger shark[38] (Galeocerdo cuvier) Ovoviviparous 430-480 10-80
Tawny nurse shark[39]: 195–199  (Nebrius ferrugineus) Aplacental viviparity 1-2
  • a Unlike any other shark, the yolk-sac placenta is globular or spherical.[39]: 380–381 
  • b At first, the embryos are sustained by a yolk sac, but later a placenta develops.
  • c A bonnethead female produced a pup by parthenogenesis in 2001.[40]
  • d The spadenose shark has the most advanced form of placental viviparity known in fish, as measured by the complexity of the placental connection and the difference in weight between the egg and the newborn young.[41]
  • e The eelpout suckles its young embryos while still within their mother's body, making it the only fish species to suckle its offspring.[27]
  • f Only one pregnant female is known to have been caught; she was carrying six unborn young.[28]
  • g 1 per uterine horn

Poeciliopsis

[edit]

Members of the genus Poeciliopsis (amongst others) show variable reproductive life history adaptations. P. monacha can be considered to be lecithotrophic because the female does not really provide any resources for her offspring after fertilization. P. lucida shows an intermediate level of matrotrophy, meaning that to a certain extent, the offspring's metabolism can actually affect the mother's metabolism, allowing for increased nutrient exchange. P. prolifica is considered to be highly matrotrophic, and almost all of the nutrients and materials needed for foetal development are supplied to the oocyte after it has been fertilized. This level of matrotrophy allows Poeciliopsis to carry several broods at different stages of development, a phenomenon known as superfetation.[42]

P. elongata, P. turneri and P. presidionis form another clade which could be considered an outgroup to the P. monacha, P.lucida, and P. prolifica clade. These three species are very highly matrotrophic – so much so that in 1947, C. L. Turner described the follicular cells of P. turneri as "pseudo-placenta, pseudo-chorion, and pseudo-allantois".[citation needed]

Guppy

[edit]

Guppies are highly prolific livebearers[43] giving birth to between five and 30 fry, though under extreme circumstances, she may give birth to only one or two or over 100. The gestation period of a guppy is typically 21–30 days, but can vary considerably. The area where a pregnant guppy's abdomen meets the tail is sometimes called the "gravid patch", or "gravid spot". When pregnant, there is a slight discoloration that slowly darkens as the guppy progresses through pregnancy. The patch first has a yellowish tinge, then brown and become deep orange as the pregnancy develops. This patch is where the fertilized eggs are stored and grow. The darkening is actually the eyes of the developing baby guppies and the orange tinge is their jelly-like eggs.[citation needed]

Elasmobranchs

[edit]

The majority of elasmobranchs are viviparous and show a wide range of strategies to provide their offspring with nourishment and respiratory requirements. Some sharks simply retain their young in the dilated posterior segment of the oviduct. In its simplest form, the uterus does not provide any additional nutrients to the embryos. However, other elasmobranchs develop secretory uterine villi that produce histotroph, a nutrient which supplements the yolk stores of the oocyte. Uterine secretions are perhaps most advanced in the stingrays. Following depletion of the yolk, the uterine lining hypertrophies into secretory appendages termed "trophonemata". The process by which the uterine secretions (also known as uterine milk or histotroph) are produced resembles that of breast milk in mammals. Furthermore, the milk is rich in protein and lipid. As the embryo grows, vascularisation of the trophonemata enlarges to form sinusoids that project out to the surface to form a functional respiratory membrane. In lamnoid sharks, following yolk use, the embryos develop teeth and eat eggs and siblings within the uterus. There is usually one fetus per uterus and it grows to enormous proportions of up to 1.3 m in length. In placental sharks, the yolk sac is not withdrawn to become incorporated into the abdominal wall. Rather, it lengthens to form an umbilical cord and the yolk sac becomes modified into a functional epitheliochorial placenta.[9]

Male pregnancy

[edit]
Pregnant male seahorse

The male fishes of seahorses, pipefishes, weedy and leafy sea dragons (Syngnathidae) are unusual as the male, rather than the female, incubates the eggs before releasing live fry into the surrounding water. To achieve this, male seahorses protect eggs in a specialized brood pouch, male sea dragons attach their eggs to a specific area on their bodies, and male pipefish of different species may do either.

When a female's eggs reach maturity, she squirts them from a chamber in her trunk via her ovipositor into his brood pouch or egg pouch, sometimes called a "marsupium". During a mammalian pregnancy, the placenta allows the female to nourish her progeny in the womb, and remove their waste products. If male pipefish and seahorses provide only a simple pouch for fish eggs to develop and hatch, it might not fully qualify as bona-fide pregnancy. However, current research suggests that in syngnathid species with well developed brood pouches, males do provide nutrients, osmoregulation and oxygenation to the embryos they carry.[44]

Seahorse

[edit]

When mating, the female seahorse deposits up to 1,500 (average of 100 to 1,000) eggs in the male's pouch, located on the ventral abdomen at the base of the tail. Male juveniles develop pouches when they are 5–7 months old. The male carries the eggs for 9 to 45 days until the seahorses emerge fully developed, but very small. The number born maybe as few as five for smaller species, or 2,500 for larger species. A male seahorse's body has large amounts of prolactin, the same hormone that governs milk production in pregnant mammals and although the male seahorse does not supply milk, his pouch provides oxygen as well as a controlled-environment.

When the fry are ready to be born, the male expels them with muscular contractions, sometimes while attaching himself to seaweed with his tail. Birth typically occurs during the night, and a female returning for the routine morning greeting finds her mate ready for the next batch of eggs.[45]

The table below shows the gestation period and number of young born for some selected seahorses.

Species Reproduction

method

Gestation period

(Days)

Number of young
Big-belly seahorse[46] (Hippocampus abdominalis) Ovoviviparous 28 600-700
Lined seahorse[47] (Hippocampus erectus) Ovoviviparous 20-21 650 (max)
Long-snouted seahorse[48] (Hippocampus guttulatus) Ovoviviparous 21 581 (max)

Pipefish

[edit]
The subcaudal pouch of the male black-striped pipefish

Pipefish brood their offspring either on distinct region of its body or in a brood pouch. Brood pouches vary significantly among different species of pipefish, but all contain a small opening through which the female's eggs can be deposited. The location of the brood pouch can be along the entire underside of the pipefish or just at the base of the tail, as with seahorses.[49] Pipefish in the genus Syngnathus have a brood pouch with a ventral seam that can completely cover all of their eggs when sealed. In males without these pouches, eggs adhere to a strip of soft skin on the ventral surface of their bodies that does not contain any exterior covering – a type of "skin brooding".[50]

At least two species of pipefish, Syngnathus fuscus and Syngnathus floridae, provide nutrients for their offspring.[51]

See also

[edit]

References

[edit]
  1. ^ a b Stölting, K.N. & Wilson, A.B. (2007). "Male pregnancy in seahorses and pipefish: beyond the mammalian model". BioEssays. 29 (9): 884–896. doi:10.1002/bies.20626. PMID 17691105. S2CID 12744225.
  2. ^ a b .Avise. J.C. & Liu, J-X. (2010). "Multiple mating and its relationship to alternative modes of gestation in male-pregnant versus female-pregnant fish species". Proceedings of the National Academy of Sciences USA. 107 (44): 18915–18920. Bibcode:2010PNAS..10718915A. doi:10.1073/pnas.1013786107. PMC 2973910. PMID 20956296.
  3. ^ a b Plaut, I. (2002). "Does pregnancy affect swimming performance of female Mosquitofish, Gambusia affinis?". Functional Ecology. 16 (3): 290–295. Bibcode:2002FuEco..16..290P. doi:10.1046/j.1365-2435.2002.00638.x.
  4. ^ a b Korsgaard, B. (1994). "Calcium metabolism in relation to ovarian functions during early and late pregnancy in the viviparous blenny Zoarces viviparus". Journal of Fish Biology. 44 (4): 661–672. Bibcode:1994JFBio..44..661K. doi:10.1111/j.1095-8649.1994.tb01242.x.
  5. ^ a b Seebacher, F.; Ward, A.J.W & Wilson, R.S. (2013). "Increased aggression during pregnancy comes at a higher metabolic cost". Journal of Experimental Biology. 216 (5): 771–776. doi:10.1242/jeb.079756. PMID 23408800.
  6. ^ Lodé, T. (2001). Les Stratégies de Reproduction des Animaux. Dunod Sciences, Paris.
  7. ^ Wourms, J.P. (1991). "Reproduction and development of Sebastes in the context of the evolution of piscine viviparity". Rockfishes of the genus Sebastes: Their reproduction and early life history. Developments in environmental biology of fishes. Vol. 30. pp. 111–126. doi:10.1007/978-94-011-3792-8_12. ISBN 978-94-010-5688-5. Retrieved November 5, 2014. {{cite book}}: |journal= ignored (help)
  8. ^ a b c Moe, M. (June 15, 2002). "The breeder's net: Science, biology, and terminology of fish reproduction: Reproductive modes and strategies-Part 1". Advanced Aquarist. Retrieved November 1, 2014.
  9. ^ a b Hamlett, W.C.; Eulitt, A.M.; Jarrell, R.L. & Kelly, M.A. (1993). "Uterogestation and placentation in elasmobranchs". Journal of Experimental Zoology. 266 (5): 347–367. doi:10.1002/jez.1402660504.
  10. ^ "Contents". The Zoo Online Fish Encyclopaedia. Retrieved November 2, 2014.
  11. ^ a b Marsh-Matthews, E.; Deaton, R. & Brooks, M. (2010). "Survey of Matrotrophy in Lecithotrophic Poeciliids" (PDF). In Uribe, M.C. & Grier, H.J. (eds.). Viviparous Fishes II. New Life Publications, Homestead, Florida. pp. 13–30. Retrieved November 1, 2014.
  12. ^ Carrier, J.C.; Musick, J.A.; Heithaus, M.R., eds. (2012). Biology of Sharks and Their Relatives. CRC Press. pp. 296–301. ISBN 978-1439839249.
  13. ^ "Surfperches". Retrieved November 2, 2014.
  14. ^ "Atlantic Sharpnose Shark". Florida Museum of Natural History. Retrieved October 16, 2014.
  15. ^ Compagno, L.J.V.; M. Dando & Fowler, S. (2005). Sharks of the World. Princeton University Press. pp. 260–261. ISBN 978-0-691-12072-0.
  16. ^ Van Der Elst, R. (1993). A Guide to the Common Sea Fishes of Southern Africa. Struik. p. 367. ISBN 9781868253944.
  17. ^ Compagno, L.J.V. (1984). Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known To Date. Food and Agriculture Organization of the United Nations.
  18. ^ "Sphyrna tiburo". Fishbase.org. Retrieved October 16, 2014.
  19. ^ McAuley, R.B.; Simpfendorfer, C.A.; Hyndes, G.A. & Lenanton, R.C.J. (2007). "Distribution and reproductive biology of the sandbar shark, Carcharhinus plumbeus (Nardo), in Western Australian waters". Mar. Freshw. Res. 58 (1): 116–126. doi:10.1071/MF05234.
  20. ^ "Butterfly goodeid". Toronto zoo. Retrieved November 2, 2014.
  21. ^ "Rhizoprionodon porosus". Fishbase.com. Retrieved October 16, 2014.
  22. ^ a b Fowler, S.L.; R.D. Cavanagh; M. Camhi; G.H. Burgess; G.M. Cailliet; S.V. Fordham; C.A. Simpfendorfer & J.A. Musick (2005). Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes. International Union for Conservation of Nature and Natural Resources. ISBN 978-2-8317-0700-6.
  23. ^ Feldheim, K. A.; Gruber, S. H.; Ashley, M. V. (August 22, 2002). "The breeding biology of lemon sharks at a tropical nursery lagoon". Proceedings of the Royal Society B: Biological Sciences. 269 (1501): 1655–1661. doi:10.1098/rspb.2002.2051. PMC 1691075. PMID 12204125.
  24. ^ Rigby, C.L.; Barreto, R.; Carlson, J.; Fernando, D.; Fordham, S.; Francis, M.P.; Herman, K.; Jabado, R.W.; Liu, K.M.; Marshall, A.; Pacoureau, N.; Romanov, E.; Sherley, R.B.; Winker, H. (2019). "Carcharhinus longimanus". IUCN Red List of Threatened Species. 2019: e.T39374A2911619. doi:10.2305/IUCN.UK.2019-3.RLTS.T39374A2911619.en. Retrieved November 12, 2021.
  25. ^ "Little seahorse". Animal Diversity web. Retrieved October 31, 2014.
  26. ^ Baremore, I.E. & Hale, L.F. (2012). "Reproduction of the sandbar shark in the Western North Atlantic Ocean and Gulf of Mexico". Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science. 4: 560–572. doi:10.1080/19425120.2012.700904.
  27. ^ a b Matt Walker (September 28, 2010). "Pregnant European eelpout fish suckles young embryos". BBC News. Retrieved October 22, 2014.
  28. ^ a b The Shark Trust. "Basking Shark Factsheet". The Shark Trust. Archived from the original on February 17, 2013. Retrieved July 7, 2006.
  29. ^ "Bat ray". Monterey Bay Aquarium Online Field Guide. Retrieved October 22, 2014.
  30. ^ Lavett Smith, C.; Rand, Charles S.; Schaeffer, Bobb; Atz, James W. (1975). "Latimeria, the living coelacanth, is ovoviviparous". Science. 190 (4219): 1105–6. Bibcode:1975Sci...190.1105L. doi:10.1126/science.190.4219.1105. S2CID 83943031.
  31. ^ Pierce, S. J.; Pardo, S. A.; Bennett, M. B. (2009). "Reproduction of the blue-spotted maskray Neotrygon kuhlii (Myliobatoidei: Dasyatidae) in south-east Queensland, Australia". Journal of Fish Biology. 74 (6): 1291–308. Bibcode:2009JFBio..74.1291P. doi:10.1111/j.1095-8649.2009.02202.x. PMID 20735632.
  32. ^ "Knifetooth sawfish". Ichthyology. Florida Museum of Natural History. Retrieved September 24, 2013.
  33. ^ Compagno, L. (2001). Sharks of the World, Vol. 2. Rome, Italy: FAO. Archived from the original on April 25, 2005. Retrieved October 25, 2014.
  34. ^ Bansemer, C.S. & Bennett, M.B. (2009). "Reproductive periodicity, localised movements and behavioural segregation of pregnant Carcharias taurus at Wolf Rock, southeast Queensland, Australia". Marine Ecology Progress Series. 374: 215–227. Bibcode:2009MEPS..374..215B. doi:10.3354/meps07741.
  35. ^ Fisheries, Staff of the Bureau of Marine (April 15, 1946). "Fish Bulletin No. 64. The Biology of the Soupfin Galeorhinus zyopterus and Biochemical Studies of the Liver". Repositories.cdlib.org. Retrieved October 28, 2014. {{cite journal}}: Cite journal requires |journal= (help)
  36. ^ Last, P.R. & Stevens, J.D. (2012). Sharks and Rays of Australia (Second ed.). Australia: CSIRO (Commonwealth Scientific and Industrial Research Organisation). ISBN 978-0-643-09457-4.
  37. ^ Kyne, P.M.; Ishihara, H.; Dudley, S.F.J. & White, W. T. (2006). "Aetobatus narinari". IUCN Red List of Threatened Species. 2006: e.T39415A10231645. doi:10.2305/IUCN.UK.2006.RLTS.T39415A10231645.en.
  38. ^ Knickle, Craig (May 8, 2017). "Galeocerdo cuvier". Ichthyology Collection, Florida Museum of Natural History, University of Florida. Retrieved March 9, 2018.
  39. ^ a b Compagno, L.J.V. (2002). Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date (Volume 2). Rome: Food and Agriculture Organization. ISBN 978-92-5-104543-5.
  40. ^ "Captive shark had 'virgin birth'". BBC. May 23, 2007.
  41. ^ Wourms, J.P. (1993). "Maximization of evolutionary trends for placental viviparity in the spadenose shark, Scoliodon laticaudus". Environmental Biology of Fishes. 38 (1–3): 269–294. Bibcode:1993EnvBF..38..269W. doi:10.1007/BF00842922. S2CID 10920369.
  42. ^ Thibault, R.E. & Schultz, R.J. (1978). "Reproductive adaptations among viviparous fishes (Cyprinodontiformes Poeciliidae)". Evolution. 32 (2): 320–333. doi:10.2307/2407600. JSTOR 2407600. PMID 28563744.
  43. ^ "Guppy". Encyclopædia Britannica Online. 2007. Archived from the original on May 13, 2008. Retrieved May 7, 2007.
  44. ^ Jones, A.G. & Avise, J.C. (2003). "Male pregnancy". Current Biology. 13 (20): R791. Bibcode:2003CBio...13.R791J. doi:10.1016/j.cub.2003.09.045. PMID 14561416. S2CID 5282823.[dead link]
  45. ^ Milius, S. (2000). "Pregnant—and still macho" (PDF). Science New Online. Retrieved October 6, 2014.
  46. ^ "Hippocampus abdominalis". Fishbase.com. Retrieved October 31, 2014.
  47. ^ "Hippocampus erectus". Retrieved October 31, 2014.
  48. ^ "Hippocampus guttulatus". Fishbase.org. Retrieved October 31, 2014.
  49. ^ Wilson, A.B.; Ahnesjö, I.; Vincent, A.C. & Meyer, A. (2003). "The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (family Syngnathidae)". Evolution. 57 (6): 1374–86. doi:10.1111/j.0014-3820.2003.tb00345.x. PMID 12894945. S2CID 16855358.
  50. ^ Jones, A.G. & Avise, J.C. (2001). "Mating systems and sexual selection in male-pregnant pipefishes and seahorses: Insights from microsatellite-based studies of maternity" (PDF). The Journal of Heredity. Retrieved November 1, 2014.[dead link]
  51. ^ Ripley, J.L. & Foran, C.M. (2009). "Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.)". J. Comp. Physiol. B. 179 (3): 325–333. doi:10.1007/s00360-008-0316-2. PMID 19005657. S2CID 22862461.